- Email: [email protected]
The epizootiology of gastrointestinal nematode parasites in Greek dairy breeds of sheep and goats
Small Ruminant Research 47 (2003) 193–202
The epizootiology of gastrointestinal nematode parasites in Greek dairy breeds of sheep and goats E. Papadopoulos a,∗ , G. Arsenos a , S. Sotiraki b , C. Deligiannis c , T. Lainas d , D. Zygoyiannis a a
School of Veterinary Medicine, Aristotle University of Thessaloniki, 54 124 Thessaloniki, Greece b Veterinary Research Institute of Thessaloniki, Thessaloniki, Greece c National Agricultural Research Foundation of Greece, Karditsa, Greece d Veterinary Services of Karditsa, Ministry of Agriculture, Karditsa, Greece Accepted 6 November 2002
Abstract Gastrointestinal (GI) parasitism represents a severe health problem in small ruminant production systems world-wide. The objective of the present study was three-fold: (i) to assess the prevalence of GI parasitism in dairy breeds of sheep and goats in selected areas of Greece; (ii) to determine the species of existing gastrointestinal parasites; and (iii) to investigate the effect of climatic factors on the seasonal variation of parasite population dynamics in dairy sheep and goats reared in two different geographical areas of Greece. The study was conducted in four flocks of either sheep or goats that were equally allocated in northern and central Greece. In each flock, faecal samples were randomly collected from 30 animals at monthly intervals and were used for nematode egg counts and coprocultures. Two animals from each flock were slaughtered monthly and their GI tract were examined for adult worm population and identification. The study revealed that the parasitic burdens in sheep were significantly (P < 0.05) higher than those in goats. Faecal egg counts for both sheep and goats were significantly (P < 0.01) affected by the month of the year and there was also a significant interaction between month of the year and area of study (P < 0.01). Teladorsagia, Haemonchus, Trichostrongylus and Chabertia were the most prevalent nematode genera in both sheep and goats. Such information could be useful for the development of strategic treatments when sheep and goats are reared under systems similar to those described in this study. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Sheep; Goats; Epizootiology; Nematodes; Greece
1. Introduction
∗ Corresponding author. Tel.: +30-31-99-99-26; fax: +30-31-99-99-47. E-mail address: [email protected] (E. Papadopoulos).
Gastrointestinal (GI) parasitism is a major health issue in small ruminant production systems and its consequences can be extensive ranging from reduced animal performance to mortality (Sykes, 1994; Waller, 1999). To a certain degree, the basic approach of
0921-4488/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 1 - 4 4 8 8 ( 0 2 ) 0 0 2 5 8 - 4
194
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
those rearing sheep and goats to control GI parasitism is blanket treatments with anthelmintics. However, such practices are now questioned because of the development of resistance by parasites to the commonly used anthelmintic products (Waller, 1997; Jackson and Coop, 2000). Combining knowledge of GI parasite epizootiology with modern anthelmintics has allowed great success on parasite control over the past decades. However, as the anthelmintic resistance of parasites to available products is increasing the need for improvement on current procedures for their control becomes a priority (Thamsborgh et al., 1999; Almeria and Uriarte, 1999). The issue of controlling GI nematodes is of particular economic importance in small ruminant production systems world-wide. Therefore, we need comprehensive information about the epizootiology of GI parasites, on a regional or national basis, and also information about variables such as host resistance, climate, and management data which can be used to adequately quantify the occurrence of disease (Niezen et al., 1996; Stromberg and Averbeck, 1999; Waller, 1999). Both sheep and goats, with emphasis on dairy production, are of major importance to southern European countries and in particular in Greece. Greece has the highest number of sheep and goats per capita in Europe with about 9 million sheep and 5.3 million goats (FAOSTAT, 2001). Both sheep and goats in Greece are reared mainly as dairy animals with meat production being considered as a by-product of lactation. The most common system of production, accounting for about 82% of the national flock, is described as semi-intensive; animal feeding is based on grazing natural pastures whereas housing and additional feeding is provided during the winter months of the year (Zygoyiannis et al., 1999). To date, the importance of infection by GI nematodes in sheep and goats in Greece has not been investigated in detail. The results described here formed part of a wider series of studies, supported by the European Commission (PL-96-1485). They were designed to investigate environmentally sensitive approaches to nematode parasite control in sustainable agricultural systems for sheep and goats. The specific objectives of the work reported in this paper were to assess the extent of GI parasitism in indigenous dairy breeds of sheep and goats reared under traditional production
systems, identify the parasitic species involved and the seasonal variation of parasite populations in such production systems. 2. Materials and methods 2.1. Animals and husbandry Four flocks, consisting of either dairy sheep or dairy goats, located at two different areas of Greece were used. These flocks were selected as being representative in terms of size of flock, genotype of animals and rearing system practised in Greece (Zygoyiannis, 1999; Zygoyiannis and Katsaounis, 1994). Two of the flocks, one rearing sheep and one goats, were located in Agios Antonios (northern Greece), a village situated about 300 m above sea level, at latitude 40◦ 26 30 N and longitude 23◦ 5 0 E. A total of 180 dairy sheep of the Karagouniko (Zakel in origin) breed comprised the sheep flock whereas the other flock consisted of 600 indigenous Greek dairy goats (Capra prisca). All animals were reared under the traditional extensive husbandry systems based on either grazing or browsing of unsupplemented hill vegetation (consisting mainly of kermes oak (Quercus coccifera) and several wild species of grass and legumes) throughout the year. In addition, from December to April, as a supplement to pasture, all the animals were given a pelleted concentrate diet, containing 180 g of crude protein (CP) and 10.5 MJ metabolisable energy (ME) per kg dry matter (DM). The other two flocks, one with dairy sheep and one with dairy goats, were located in Karditsa (central Greece), situated about 112 m above sea level, at latitude 39◦ 26 N and longitude 22◦ 15 E. One of the flocks consisted of 220 sheep and the other of 240 goats, respectively. They were of the same origin as those animals in the flocks in northern Greece. The animals of these flocks were kept under the same husbandry conditions as those in the two flocks in northern Greece. However, during the critical winter period (December–April) the concentrate mixture that was offered contained 170 g CP and 11.5 MJ ME per kg DM. The lambing/kidding period for all animals from both areas of study lasted from early December to January. None of the animal used in the present study
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
was given any anthelmintic treatment for at least 10 months prior to the start of the experiment. 2.2. Measurements 2.2.1. Meteorological data Meteorological data were collected, throughout the experimental period from both areas of study, including mean monthly temperatures (minimum and maximum in ◦ C), precipitation (in mm) and relative humidity (%). 2.2.2. Faecal examination Faecal samples were taken monthly for a period of 12 months from the rectum of 30 (10 adult male, 10 adult female and 10 female yearling) animals from each flock that were randomly selected at each sampling. All samples were examined individually for GI nematode eggs (faecal egg counts, FEC) using the modified McMaster technique (each count represents 50 eggs/g). The FEC were expressed as number of eggs/g fresh faeces (MAFF, 1986). 2.2.3. Necropsies Two animals (adult females) from each flock were slaughtered every month, throughout the experiment. Their GI tract was removed and examined for adult worm recovery and identification (MAFF, 1986). 2.2.4. Coprocultures The faecal samples collected from each group within a flock were pooled, stored in an isothermal container and cultured within the same or the next day. The latter was repeated at a monthly basis, for the third stage larvae identification (MAFF, 1986). This was done in order to determine the most important parasitic genera that were expressed as percentage of the total population of each group. 2.3. Statistical analysis All statistical analyses were performed using Genstat 5 (Lawes Agricultural Trust, 1993). Values of FEC and larvae genera were treated as repeated measurement data using a split-plot model of analyses of variance with group as the main plot and the months of the year as the sub-plot. Using a similar model, month, sex of animals and the geographic area where
195
the flock was located, were used as factors for the analysis. Effects of geographic area and sex were tested overall and month effects and interactions of month with geographic area and sex were tested over month. As adult worms data were collected from different animals each month, these was treated as independent and so effects of geographic area, month and their interaction were tested at the individual animal level. Prior to the analyses, the values of FEC and adult worms were log-transformed (using log(x + 1)) to stabilise the variance whereas larvae counts were √ arcsine-transformed (using arcsine x/100), as they were percentages. Back-transformed mean values are reported in Section 3. 3. Results 3.1. Meteorological data The meteorological data (mean monthly temperatures, precipitation and relative humidity) of the two areas of study are shown in Fig. 1a and b, respectively. Mean monthly temperatures for both areas were similar, however, in the central part of Greece more extreme temperatures were observed. The lowest and highest temperatures recorded in central Greece were −6 and +42 ◦ C and in northern Greece +2.1 and +31.1 ◦ C, respectively. The hottest months of the year for both areas were June and July and the coldest February. The rainfall pattern was also similar in both areas, but the precipitation in central Greece was higher than that in northern Greece. 3.2. Prevalence and monthly pattern of nematodes The faecal egg counts (FEC) of sheep and goats from flocks located either in northern or central Greece are shown in Fig. 2. FEC of sheep did not differ significantly between the two areas and between sexes. However, FEC from both areas were significantly affected by month of the year (P < 0.01). There was a significant interaction between month of the year and area (P < 0.01); this was due to the fact that the FEC of both sheep and goats in flocks of northern Greece were significantly lower in January and higher in June than the ones in central Greece, respectively.
196
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
Fig. 1. Values of precipitation, humidity and temperature (minimum and maximum) in: (a) northern Greece; (b) central Greece.
The peak of the FEC in the northern Greece was in April whereas in central Greece the peak was observed in March. The lowest FEC counts for sheep in the northern Greece were observed in January, but for the sheep of central Greece in June (Fig. 2). FEC of goats were affected by month of the year (P < 0.001), but there was not any significant difference or interaction between the two geographic areas or the sex of animals (Fig. 2).
3.3. Worm burdens of sheep and goats The most prevalent worms were Teladorsagia circumcincta, Haemonchus contortus, Trichostrongylus colubriformis and Chabertia ovina. Their mean back-transformed values are presented in Tables 1 and 2. The number of adult H. contortus worm counts in sheep from both areas were significantly affected by the month of the year (P < 0.001). In northern
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
197
Fig. 2. Faecal egg counts (FEC) of sheep and goats from flocks located either in northern or central Greece.
Greece, the highest number of H. contortus worms were recorded in March and August, and the lowest in January and December. In central Greece, the higher number of this worm were recorded in March and April, while the lowest in January. No effect was observed on any other adult worm species recovered from sheep GI tracts. There was also a significant interaction between area and month on adult T. circumcincta worm counts of goats (P < 0.05). T. circumcincta worms of goats were significantly higher in the northern rather than in central Greece in April and June. The rest of the adult worm burdens of goats were not significantly affected by month, sex or area of the study. Tables 1 and 2 show the back-transformed mean percentages of the most important larval genera from sheep and goats, respectively. There was a significant effect of month on the percentages of the larval genera Teladorsagia, Haemonchus and Chabertia in sheep (P < 0.001). Moreover, the population of Trichostrongylus spp. larvae was affected by month; however, such differences were not significant (P > 0.05). The highest percentages of Teladorsagia spp. were observed in January, February and December, and the lowest in July. Haemonchus spp. percentages were highest in June–August, while lowest in November–January. Chabertia spp. percentages were highest in July and August, while the lowest observed
in January. Moreover, Trichostrongylus spp. were highest in September and lowest in February. There were no significant differences between the two geographic areas of study except for the larvae of Teladorsagia spp. in northern Greece, where the percentages tended to be higher than in central Greece (P > 0.05). However, there was a significant interaction between geographic area and month of the year on the larval genus of Haemonchus (P < 0.01); percentages were higher in northern Greece during February and July and in central Greece during September and October. Although not statistically significant (P > 0.05) the observed percentages of Chabertia spp. in central Greece tended to be higher in March, April and July. In goats, a significant month effect was found on the percentages of Teladorsagia spp. larvae (P < 0.05), with higher percentages in March and July and lower in June and August. There was a significant interaction (P < 0.05) between month of the year and area of study, suggesting that the higher percentages were observed in central Greece for January and May, and the latter accounted also for the significant interaction (P < 0.05) between month and sex. There were not any other significant effects or interactions for the rest of the larval genera identified in the coprocultures of goats. Some other nematodes that have been also recovered were Cooperia spp., Nematodirus spp. and Oesophagostomum spp. However, these were in minor
198
Area
Parasites
January
February
March
April
June
325 (59.7) 138 (11.0) 858 (11.7)
534 (57.9) 215 (19.5) 3787 (0.915)
July
September
Central
970 (57.9) 449 (19.1) 442 (10.4)
1342 (59.3) 702 (16.1) 989 (11.8)
322 (53.1) 174 (16.3) 361 (18.1)
389 (64.6) 123 (15.7) 380 (13.7)
1144 (46.7) 222 (10.8) 805 (17.7)
225 (58.1) 310 (15.3) 807 (13.9)
500 (46.9) 158 (18.0) 856 (24.9)
804 (68.9) 85 (8.88) 399 (19.0)
363 (3.04)
325 (1.74)
268 (9.44)
351 (3.35)
356 (20.1)
248 (3.73)
351 (1.41)
188 (0.043)
60 (0.027)
89 (0.079)
838 (5.73)
770 (62.7) 780 (64.0) 300 (18.6) 85 (9.53) 444 (0.058) 415 (20.9)
October
405 (88.3) 341 (11.2) 454 (0.023) 150 (0.001)
575 (58.3) 149 (22.4) 815 (2.16)
August
Northern Teladorsagia spp. 339 (97.7) 500 (84.1) Haemonchus spp. 19 (0.292) 133 (8.48) Trichostrongylus 119 (0.820) 129 (1.89) spp. Chabertia spp. 28 (0.001) 0 (0.035) Teladorsagia spp. 411 (95.0) 692 (97.0) Haemonchus spp. 0 (0.018) 64 (0.009) Trichostrongylus 174 (1.70) 324 (0.382) spp. Chabertia spp. 48 (0.001) 80 (0.001)
641 (62.3) 182 (10.4) 382 (22.6)
May
222 (0.071) 448 (12.0)
Values in parenthesis represent percentages of larval nematodes. These third stage larvae were cultured and identified from faecal samples.
November
December
688 (92.0) 600 (82.8) 845 (95.7) 19 (0.463) 116 (0.038) 72 (0.01) 212 (5.60) 298 (14.9) 352 (0.593)
133 (0.633) 133 (0.001)
0 (0.028) 116 (0.187) 567 (94.6) 412 (92.1) 12 (0.011) 48 (0.013) 439 (2.16) 276 (3.33) 12 (0.001)
0 (0.001)
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
Table 1 Back-transformed mean values of gastrointestinal adult nematode counts and larval nematode percentages of dairy sheep from northern and central Greece
Area
Parasites
January
February
March
April
May
Northern Teladorsagia spp. Haemonchus spp. Trichostrongylus spp. Chabertia spp.
2931 (62.3) 949 (64.5) 325 (22.1) 1034 (22.7) 0 (2.74) 0 (3.88)
Central
2696 (74.2) 1972 (69.6) 2498 (75.3) 2222 (62.6) 3249 (79.0) 263 (15.7) 79 (21.1) 0 (9.66) 666 (25.3) 101 (17.4) 0 (3.35) 0 (0.357) 666 (5.07) 37 (0.357) 0 (0.585)
Teladorsagia spp. Haemonchus spp. Trichostrongylus spp. Chabertia spp.
159 (5.04)
666 (2.45)
45 (6.47)
779 (5.27)
June
1342 (68.6) 4524 (63.3) 2373 (56.8) 4092 (63.1) 19 (24.4) 133 (21.6) 0 (24.5) 0 (14.9) 48 (1.42) 0 (0.346) 101 (0.998) 0 (8.37) 169 (3.60)
125 (3.85)
256 (12.2)
100 (5.83)
0 (9.37)
435 (1.70)
208 (8.65)
July 3410 (70.9) 0 (19.5) 0 (0.023) 666 (7.21)
153 (60.4) 2436 (76.1) 5 (25.3) 12 (14.6) 0 (0.332) 19 (5.28) 169 (8.85)
0 (0.541)
August
September
651 (63.1) 3848 (70.2) 0 (19.6) 1080 (18.1) 0 (5.14) 28 (1.41) 101 (5.32)
544 (7.24)
2048 (60.7) 2151 (70.5) 37 (14.2) 133 (16.4) 0 (6.92) 0 (8.03) 72 (10.2)
Values in parenthesis represent percentages of larval nematodes. These third stage larvae were cultured and identified from faecal samples.
October 894 (69.2) 101 (21.4) 72 (0.03) 4083 (5.16)
November
28 (9.12)
2218 (66.9) 1095 (64.1) 28 (18.5) 12 (17.3) 528 (0.037) 0 (0.579)
261 (0.509) 1034 (9.75)
December
941 (67.1) 2974 (64.2) 169 (17.1) 48 (17.6) 275 (0.056) 28 (6.52)
3806 (7.38)
143 (7.58) 529 (64.0) 37 (17.4) 304 (3.66) 116 (7.91)
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
Table 2 Back-transformed mean values of gastrointestinal adult nematode counts and larval nematode percentages of dairy goats from flocks in northern and central Greece
199
200
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
percentages, therefore they were not included in the statistical analysed.
4. Discussion The comprehensive knowledge of the epizootiology of parasitism is a crucial requirement to the sustainable control of nematodes, as it interacts with the host in a specific climatic, management and production environment (Almeria and Uriarte, 1999; Waller, 1999). Anthelmintic resistance of nematode parasites of sheep and goats is present world-wide, including Greece (Papadopoulos et al., 2001), and threatens the future viability of small ruminant production in many countries (Jackson, 1993; Waller, 1999; Hoste et al., 2001). This high incidence of anthelmintic resistance is forcing people either to adopt alternative control strategies or to greatly modify the existing ones. The design of successful sustainable parasite control programmes requires knowledge of the dynamics of egg shedding from the host, seasonal larval availability together with information about climatic requirements for worm egg hatching, larval development and survival at pasture (Barger, 1999; Stromberg and Averbeck, 1999; Nginyi et al., 2001). In our study, sheep and goats from both areas were expelling nematode eggs throughout the studied period. However, this egg output was significantly different between different months of the year. Sheep from both areas of Greece had significantly higher FEC than goats. The peak of FEC of sheep was observed in April and March for northern and central Greece, respectively. This peak was noted earlier than the ones reported in other regions of northern and central Greece (Theodoropoulos et al., 1998, 2000), where FEC peaks were observed during summer. This might be due to local management differences in those areas or to different susceptibility to nematode infection of sheep used in those experiments. In our study, the intensity of infection with GI nematodes in both sheep and goats started to increase after February and the highest FEC were observed during spring. This might be associated with the post-partum or spring egg rise. However, the subsequent decrease of FEC may be affected by the development of host immunity, as a result of better nutrition during spring and the beginning of summer, or it might be related, especially to
younger animals, to the level of larval ingestion which is conditioned by the host feeding behaviour during grazing. A second but smaller peak of FEC, for both sheep and goats, was observed in October. In our view, the latter might be due to the re-infection of animals because of increased rainfall during this season that provided a more suitable environment for the survival of nematodes infective larvae, which consequently became a source of infection for the grazing animals. This higher faecal egg production during spring and autumn is well correlated with increased rainfall, particularly in central Greece, and therefore the presence of green vegetation. On the other hand, during the hot and dry summer the animals have to face the shortage of the green vegetation, which however is associated with less risk of GI nematode infection because larvae do not easily survive under such climatic conditions. Hence, it seems that rainfall is likely to be more closely correlated with the level of GI nematode parasitism than other factors, such as flock management (Cabaret et al., 1989; Niezen et al., 1996). Based on results of both the coprocultures and necropsies, we suggest that Teladorsagia is the most prevalent worm genus present throughout the year in both areas of Greece, and therefore plays an important role in the parasitic gastroenteritis together with Trichostrongylus spp., Haemonchus spp. and Chabertia spp. The less prevalent genera were Cooperia, Nematodirus and Oesophagostomum. The parasites recovered in our study have been previously reported in other surveys taken place in Greece (Theodoridis and Himonas, 1990; Papadopoulos, 1997; Theodoridis et al., 2000; Theodoropoulos et al., 2000; Papadopoulos et al., 2001). It is worth noting that in Greece, up to now, only T. circumcincta has been found to be anthelmintic resistant (Papadopoulos et al., 2001). Anthelmintic treatments of small ruminants in Greece are carried out usually once or twice per year. The present data could provide a concise epizootiological picture of gastrointestinal strongyles of small ruminants in Greece, and based on these finding we can make some recommendations regarding the anthelmintic treatment of grazing animals. The most appropriate time for treatment, according to our findings, seems to be the end of winter—beginning of spring before the peak of FEC occurs. Treatment at this time will also prevent the development of disease and any clinical symptoms in either ewes or lambs.
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
It should be noted here that under traditional small ruminant production systems in Greece, animals are not separated according to age groups but are reared together as a flock. The benefits of treating ewes at parturition, when milk is consumed by new-borns or earlier during dry period (pregnancy) are higher milk production and avoidance of withdrawal periods of milk due to drug residues period. If second treatment is needed, then treating animals during summer, when due to the drought the only surviving worms are the ones in the host, might offer a good chance to kill these worms. Furthermore, this would allow minimum contamination of the pasture and prevent the build up of worm burdens in the hosts. Nevertheless, in the latter case, it is important to note that care should be taken since the selection pressure for anthelmintic resistance is higher and any treatment should be applied with caution. According to our results, goats do not have high FEC, and therefore seem not to urgently need any anthelmintic treatment at all. We suggest that the observed differences in the FEC between sheep and goats might be due to host susceptibility and grazing behaviour of such animals (Hoste et al., 2001). Results of the current study provide a further understanding of the factors associated with parasite epizootiology and the relationship between the parasites and their host. Such information could be useful for the development of strategic treatments when sheep and goats are reared under systems similar to those described in this study.
Acknowledgements The work was supported by the European Commission (DG VI) project No. FAIR 3-CT96-1485, as part of a collaborative programme between the UK, France, Greece and Spain. We would like to thank Dr. D. Allcroft of SAC, Edinburgh, for his helpful comments on how to improve the manuscript. References Almeria, S., Uriarte, J., 1999. Dynamics of pasture contamination by gastrointestinal nematodes of cattle under extensive management systems: proposal for strategic control. Vet. Parasitol. 83, 37–47.
201
Barger, I., 1999. The role of epidemiological knowledge and grazing management for helminth control in small ruminants. Int. J. Parasitol. 29, 41–47. Cabaret, J., Anjorand, N., Leclerc, C., 1989. Parasitic risk factors on pastures of French dairy goat farms. Small Rumin. Res. 2, 69–78. FAOSTAT, 2001. FAO Agriculture Statistical Database. Hoste, H., Leveque, H., Dorchies, Ph., 2001. Comparison of nematode infections of the gastrointestinal tract in Angora and dairy goats in a rangeland environment: relations with the feeding behaviour. Vet. Parasitol. 101, 127–135. Jackson, F., 1993. Anthelmintic resistance—the state of play. Brit. Vet. J. 149, 123–138. Jackson, F., Coop, R.L., 2000. The development of anthelmintic resistance in sheep nematodes. Parasitology 120, S95–S107. Lawes Agricultural Trust, 1993. Genstat 5 Release 3.2 Reference Manual, 2nd ed. Clarendon Press, Oxford. Ministry of Agriculture Fisheries and Food (MAFF), 1986. Manual of Veterinary Parasitological Laboratory Techniques. Reference Book 418. HMSO, London. Nginyi, J.M., Duncan, J.L., Mellor, D.J., Stear, M.J., Wanyangu, S.W., Bain, R.K., Gatongi, P.M., 2001. Epidemiology of parasitic gastrointestinal nematode infections of ruminants on smallholder farms in central Kenya. Res. Vet. Sci. 70, 33– 39. Niezen, J.H., Charleston, W.A.G., Hodgson, J., McKay, A.D., Leathwick, D.M., 1996. Controlling internal parasites in grazing ruminants without recourse to anthelmintics: approaches, experiences, prospects. Int. J. Parasitol. 26, 983–992. Papadopoulos, E., 1997. Anthelmintic resistance of sheep and goat gastrointestinal nematode parasites in Greece. Doctoral thesis, Aristotle University of Thessaloniki, Greece. Papadopoulos, E., Himonas, C., Coles, G.C., 2001. Drought and flock isolation may enhance the development of anthelmintic resistance in nematodes. Vet. Parasitol. 97, 89–93. Stromberg, B., Averbeck, G., 1999. The role of parasite epidemiology in the management of grazing cattle. Int. J. Parasitol. 29, 33–39. Sykes, A.R., 1994. Parasitism and production in farm animals. Anim. Prod. 59, 155–172. Thamsborgh, M.S., Roepstorff, A., Larsen, M., 1999. Integrated and biological control of parasites in organic and conventional production systems. Vet. Parasitol. 84, 169–186. Theodoridis, Y., Himonas, C., 1990. A survey on the specific aetiology of sheep and goats gastrointestinal nematodosis. In: Proceedings of the Fifth Hellenic Veterinary Congress, Thessaloniki, Greece, 22–25 November 1990, pp. 96–98 (Abstract No. E-6). Theodoridis, Y., Himonas, C., Papazahariadou, M., 2000. Helminths parasites of digestive tract of sheep and goats in Macedonian region. Bull. Hellenic Vet. Med. Soc. 51, 195–199. Theodoropoulos, G., Koutsotolis, K., Nikolaou, E., Kalogiannis, D., Petrakos, G., 1998. Seasonal variation of gastrointestinal nematodes of sheep in the region of Joannina, Greece. Int. J. Parasitol. 28, 1287–1292. Theodoropoulos, G., Zervas, G., Kouneli, A., Martinez-Gonzales, B., Petrakos, G., Kostopoulos, J., 2000. Seasonal patterns of
202
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
strongyle infections in grazing sheep under the traditional production system in the region of Trikala, Greece. Vet. Parasitol. 89, 327–335. Waller, P.J., 1997. Anthelmintic resistance. Vet. Parasitol. 72, 391– 412. Waller, P.J., 1999. International approaches to the concept of integrated control of nematode parasites of livestock. Int. J. Parasitol. 29, 155–164.
Zygoyiannis, D., 1999. Sheep Production. Modern Education, Thessaloniki. Zygoyiannis, D., Katsaounis, N., 1994. Goat Production. Modern Education, Thessaloniki. Zygoyiannis, D., Katsaounis, N., Stamataris, C., Arsenos, G., Tsaras, L., Doney, J., 1999. The use of nutritional management after weaning for the production of heavier lamb carcasses from Greek dairy breeds. Livest. Prod. Sci. 57, 279–289.
The epizootiology of gastrointestinal nematode parasites in Greek dairy breeds of sheep and goats E. Papadopoulos a,∗ , G. Arsenos a , S. Sotiraki b , C. Deligiannis c , T. Lainas d , D. Zygoyiannis a a
School of Veterinary Medicine, Aristotle University of Thessaloniki, 54 124 Thessaloniki, Greece b Veterinary Research Institute of Thessaloniki, Thessaloniki, Greece c National Agricultural Research Foundation of Greece, Karditsa, Greece d Veterinary Services of Karditsa, Ministry of Agriculture, Karditsa, Greece Accepted 6 November 2002
Abstract Gastrointestinal (GI) parasitism represents a severe health problem in small ruminant production systems world-wide. The objective of the present study was three-fold: (i) to assess the prevalence of GI parasitism in dairy breeds of sheep and goats in selected areas of Greece; (ii) to determine the species of existing gastrointestinal parasites; and (iii) to investigate the effect of climatic factors on the seasonal variation of parasite population dynamics in dairy sheep and goats reared in two different geographical areas of Greece. The study was conducted in four flocks of either sheep or goats that were equally allocated in northern and central Greece. In each flock, faecal samples were randomly collected from 30 animals at monthly intervals and were used for nematode egg counts and coprocultures. Two animals from each flock were slaughtered monthly and their GI tract were examined for adult worm population and identification. The study revealed that the parasitic burdens in sheep were significantly (P < 0.05) higher than those in goats. Faecal egg counts for both sheep and goats were significantly (P < 0.01) affected by the month of the year and there was also a significant interaction between month of the year and area of study (P < 0.01). Teladorsagia, Haemonchus, Trichostrongylus and Chabertia were the most prevalent nematode genera in both sheep and goats. Such information could be useful for the development of strategic treatments when sheep and goats are reared under systems similar to those described in this study. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Sheep; Goats; Epizootiology; Nematodes; Greece
1. Introduction
∗ Corresponding author. Tel.: +30-31-99-99-26; fax: +30-31-99-99-47. E-mail address: [email protected] (E. Papadopoulos).
Gastrointestinal (GI) parasitism is a major health issue in small ruminant production systems and its consequences can be extensive ranging from reduced animal performance to mortality (Sykes, 1994; Waller, 1999). To a certain degree, the basic approach of
0921-4488/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 1 - 4 4 8 8 ( 0 2 ) 0 0 2 5 8 - 4
194
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
those rearing sheep and goats to control GI parasitism is blanket treatments with anthelmintics. However, such practices are now questioned because of the development of resistance by parasites to the commonly used anthelmintic products (Waller, 1997; Jackson and Coop, 2000). Combining knowledge of GI parasite epizootiology with modern anthelmintics has allowed great success on parasite control over the past decades. However, as the anthelmintic resistance of parasites to available products is increasing the need for improvement on current procedures for their control becomes a priority (Thamsborgh et al., 1999; Almeria and Uriarte, 1999). The issue of controlling GI nematodes is of particular economic importance in small ruminant production systems world-wide. Therefore, we need comprehensive information about the epizootiology of GI parasites, on a regional or national basis, and also information about variables such as host resistance, climate, and management data which can be used to adequately quantify the occurrence of disease (Niezen et al., 1996; Stromberg and Averbeck, 1999; Waller, 1999). Both sheep and goats, with emphasis on dairy production, are of major importance to southern European countries and in particular in Greece. Greece has the highest number of sheep and goats per capita in Europe with about 9 million sheep and 5.3 million goats (FAOSTAT, 2001). Both sheep and goats in Greece are reared mainly as dairy animals with meat production being considered as a by-product of lactation. The most common system of production, accounting for about 82% of the national flock, is described as semi-intensive; animal feeding is based on grazing natural pastures whereas housing and additional feeding is provided during the winter months of the year (Zygoyiannis et al., 1999). To date, the importance of infection by GI nematodes in sheep and goats in Greece has not been investigated in detail. The results described here formed part of a wider series of studies, supported by the European Commission (PL-96-1485). They were designed to investigate environmentally sensitive approaches to nematode parasite control in sustainable agricultural systems for sheep and goats. The specific objectives of the work reported in this paper were to assess the extent of GI parasitism in indigenous dairy breeds of sheep and goats reared under traditional production
systems, identify the parasitic species involved and the seasonal variation of parasite populations in such production systems. 2. Materials and methods 2.1. Animals and husbandry Four flocks, consisting of either dairy sheep or dairy goats, located at two different areas of Greece were used. These flocks were selected as being representative in terms of size of flock, genotype of animals and rearing system practised in Greece (Zygoyiannis, 1999; Zygoyiannis and Katsaounis, 1994). Two of the flocks, one rearing sheep and one goats, were located in Agios Antonios (northern Greece), a village situated about 300 m above sea level, at latitude 40◦ 26 30 N and longitude 23◦ 5 0 E. A total of 180 dairy sheep of the Karagouniko (Zakel in origin) breed comprised the sheep flock whereas the other flock consisted of 600 indigenous Greek dairy goats (Capra prisca). All animals were reared under the traditional extensive husbandry systems based on either grazing or browsing of unsupplemented hill vegetation (consisting mainly of kermes oak (Quercus coccifera) and several wild species of grass and legumes) throughout the year. In addition, from December to April, as a supplement to pasture, all the animals were given a pelleted concentrate diet, containing 180 g of crude protein (CP) and 10.5 MJ metabolisable energy (ME) per kg dry matter (DM). The other two flocks, one with dairy sheep and one with dairy goats, were located in Karditsa (central Greece), situated about 112 m above sea level, at latitude 39◦ 26 N and longitude 22◦ 15 E. One of the flocks consisted of 220 sheep and the other of 240 goats, respectively. They were of the same origin as those animals in the flocks in northern Greece. The animals of these flocks were kept under the same husbandry conditions as those in the two flocks in northern Greece. However, during the critical winter period (December–April) the concentrate mixture that was offered contained 170 g CP and 11.5 MJ ME per kg DM. The lambing/kidding period for all animals from both areas of study lasted from early December to January. None of the animal used in the present study
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
was given any anthelmintic treatment for at least 10 months prior to the start of the experiment. 2.2. Measurements 2.2.1. Meteorological data Meteorological data were collected, throughout the experimental period from both areas of study, including mean monthly temperatures (minimum and maximum in ◦ C), precipitation (in mm) and relative humidity (%). 2.2.2. Faecal examination Faecal samples were taken monthly for a period of 12 months from the rectum of 30 (10 adult male, 10 adult female and 10 female yearling) animals from each flock that were randomly selected at each sampling. All samples were examined individually for GI nematode eggs (faecal egg counts, FEC) using the modified McMaster technique (each count represents 50 eggs/g). The FEC were expressed as number of eggs/g fresh faeces (MAFF, 1986). 2.2.3. Necropsies Two animals (adult females) from each flock were slaughtered every month, throughout the experiment. Their GI tract was removed and examined for adult worm recovery and identification (MAFF, 1986). 2.2.4. Coprocultures The faecal samples collected from each group within a flock were pooled, stored in an isothermal container and cultured within the same or the next day. The latter was repeated at a monthly basis, for the third stage larvae identification (MAFF, 1986). This was done in order to determine the most important parasitic genera that were expressed as percentage of the total population of each group. 2.3. Statistical analysis All statistical analyses were performed using Genstat 5 (Lawes Agricultural Trust, 1993). Values of FEC and larvae genera were treated as repeated measurement data using a split-plot model of analyses of variance with group as the main plot and the months of the year as the sub-plot. Using a similar model, month, sex of animals and the geographic area where
195
the flock was located, were used as factors for the analysis. Effects of geographic area and sex were tested overall and month effects and interactions of month with geographic area and sex were tested over month. As adult worms data were collected from different animals each month, these was treated as independent and so effects of geographic area, month and their interaction were tested at the individual animal level. Prior to the analyses, the values of FEC and adult worms were log-transformed (using log(x + 1)) to stabilise the variance whereas larvae counts were √ arcsine-transformed (using arcsine x/100), as they were percentages. Back-transformed mean values are reported in Section 3. 3. Results 3.1. Meteorological data The meteorological data (mean monthly temperatures, precipitation and relative humidity) of the two areas of study are shown in Fig. 1a and b, respectively. Mean monthly temperatures for both areas were similar, however, in the central part of Greece more extreme temperatures were observed. The lowest and highest temperatures recorded in central Greece were −6 and +42 ◦ C and in northern Greece +2.1 and +31.1 ◦ C, respectively. The hottest months of the year for both areas were June and July and the coldest February. The rainfall pattern was also similar in both areas, but the precipitation in central Greece was higher than that in northern Greece. 3.2. Prevalence and monthly pattern of nematodes The faecal egg counts (FEC) of sheep and goats from flocks located either in northern or central Greece are shown in Fig. 2. FEC of sheep did not differ significantly between the two areas and between sexes. However, FEC from both areas were significantly affected by month of the year (P < 0.01). There was a significant interaction between month of the year and area (P < 0.01); this was due to the fact that the FEC of both sheep and goats in flocks of northern Greece were significantly lower in January and higher in June than the ones in central Greece, respectively.
196
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
Fig. 1. Values of precipitation, humidity and temperature (minimum and maximum) in: (a) northern Greece; (b) central Greece.
The peak of the FEC in the northern Greece was in April whereas in central Greece the peak was observed in March. The lowest FEC counts for sheep in the northern Greece were observed in January, but for the sheep of central Greece in June (Fig. 2). FEC of goats were affected by month of the year (P < 0.001), but there was not any significant difference or interaction between the two geographic areas or the sex of animals (Fig. 2).
3.3. Worm burdens of sheep and goats The most prevalent worms were Teladorsagia circumcincta, Haemonchus contortus, Trichostrongylus colubriformis and Chabertia ovina. Their mean back-transformed values are presented in Tables 1 and 2. The number of adult H. contortus worm counts in sheep from both areas were significantly affected by the month of the year (P < 0.001). In northern
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
197
Fig. 2. Faecal egg counts (FEC) of sheep and goats from flocks located either in northern or central Greece.
Greece, the highest number of H. contortus worms were recorded in March and August, and the lowest in January and December. In central Greece, the higher number of this worm were recorded in March and April, while the lowest in January. No effect was observed on any other adult worm species recovered from sheep GI tracts. There was also a significant interaction between area and month on adult T. circumcincta worm counts of goats (P < 0.05). T. circumcincta worms of goats were significantly higher in the northern rather than in central Greece in April and June. The rest of the adult worm burdens of goats were not significantly affected by month, sex or area of the study. Tables 1 and 2 show the back-transformed mean percentages of the most important larval genera from sheep and goats, respectively. There was a significant effect of month on the percentages of the larval genera Teladorsagia, Haemonchus and Chabertia in sheep (P < 0.001). Moreover, the population of Trichostrongylus spp. larvae was affected by month; however, such differences were not significant (P > 0.05). The highest percentages of Teladorsagia spp. were observed in January, February and December, and the lowest in July. Haemonchus spp. percentages were highest in June–August, while lowest in November–January. Chabertia spp. percentages were highest in July and August, while the lowest observed
in January. Moreover, Trichostrongylus spp. were highest in September and lowest in February. There were no significant differences between the two geographic areas of study except for the larvae of Teladorsagia spp. in northern Greece, where the percentages tended to be higher than in central Greece (P > 0.05). However, there was a significant interaction between geographic area and month of the year on the larval genus of Haemonchus (P < 0.01); percentages were higher in northern Greece during February and July and in central Greece during September and October. Although not statistically significant (P > 0.05) the observed percentages of Chabertia spp. in central Greece tended to be higher in March, April and July. In goats, a significant month effect was found on the percentages of Teladorsagia spp. larvae (P < 0.05), with higher percentages in March and July and lower in June and August. There was a significant interaction (P < 0.05) between month of the year and area of study, suggesting that the higher percentages were observed in central Greece for January and May, and the latter accounted also for the significant interaction (P < 0.05) between month and sex. There were not any other significant effects or interactions for the rest of the larval genera identified in the coprocultures of goats. Some other nematodes that have been also recovered were Cooperia spp., Nematodirus spp. and Oesophagostomum spp. However, these were in minor
198
Area
Parasites
January
February
March
April
June
325 (59.7) 138 (11.0) 858 (11.7)
534 (57.9) 215 (19.5) 3787 (0.915)
July
September
Central
970 (57.9) 449 (19.1) 442 (10.4)
1342 (59.3) 702 (16.1) 989 (11.8)
322 (53.1) 174 (16.3) 361 (18.1)
389 (64.6) 123 (15.7) 380 (13.7)
1144 (46.7) 222 (10.8) 805 (17.7)
225 (58.1) 310 (15.3) 807 (13.9)
500 (46.9) 158 (18.0) 856 (24.9)
804 (68.9) 85 (8.88) 399 (19.0)
363 (3.04)
325 (1.74)
268 (9.44)
351 (3.35)
356 (20.1)
248 (3.73)
351 (1.41)
188 (0.043)
60 (0.027)
89 (0.079)
838 (5.73)
770 (62.7) 780 (64.0) 300 (18.6) 85 (9.53) 444 (0.058) 415 (20.9)
October
405 (88.3) 341 (11.2) 454 (0.023) 150 (0.001)
575 (58.3) 149 (22.4) 815 (2.16)
August
Northern Teladorsagia spp. 339 (97.7) 500 (84.1) Haemonchus spp. 19 (0.292) 133 (8.48) Trichostrongylus 119 (0.820) 129 (1.89) spp. Chabertia spp. 28 (0.001) 0 (0.035) Teladorsagia spp. 411 (95.0) 692 (97.0) Haemonchus spp. 0 (0.018) 64 (0.009) Trichostrongylus 174 (1.70) 324 (0.382) spp. Chabertia spp. 48 (0.001) 80 (0.001)
641 (62.3) 182 (10.4) 382 (22.6)
May
222 (0.071) 448 (12.0)
Values in parenthesis represent percentages of larval nematodes. These third stage larvae were cultured and identified from faecal samples.
November
December
688 (92.0) 600 (82.8) 845 (95.7) 19 (0.463) 116 (0.038) 72 (0.01) 212 (5.60) 298 (14.9) 352 (0.593)
133 (0.633) 133 (0.001)
0 (0.028) 116 (0.187) 567 (94.6) 412 (92.1) 12 (0.011) 48 (0.013) 439 (2.16) 276 (3.33) 12 (0.001)
0 (0.001)
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
Table 1 Back-transformed mean values of gastrointestinal adult nematode counts and larval nematode percentages of dairy sheep from northern and central Greece
Area
Parasites
January
February
March
April
May
Northern Teladorsagia spp. Haemonchus spp. Trichostrongylus spp. Chabertia spp.
2931 (62.3) 949 (64.5) 325 (22.1) 1034 (22.7) 0 (2.74) 0 (3.88)
Central
2696 (74.2) 1972 (69.6) 2498 (75.3) 2222 (62.6) 3249 (79.0) 263 (15.7) 79 (21.1) 0 (9.66) 666 (25.3) 101 (17.4) 0 (3.35) 0 (0.357) 666 (5.07) 37 (0.357) 0 (0.585)
Teladorsagia spp. Haemonchus spp. Trichostrongylus spp. Chabertia spp.
159 (5.04)
666 (2.45)
45 (6.47)
779 (5.27)
June
1342 (68.6) 4524 (63.3) 2373 (56.8) 4092 (63.1) 19 (24.4) 133 (21.6) 0 (24.5) 0 (14.9) 48 (1.42) 0 (0.346) 101 (0.998) 0 (8.37) 169 (3.60)
125 (3.85)
256 (12.2)
100 (5.83)
0 (9.37)
435 (1.70)
208 (8.65)
July 3410 (70.9) 0 (19.5) 0 (0.023) 666 (7.21)
153 (60.4) 2436 (76.1) 5 (25.3) 12 (14.6) 0 (0.332) 19 (5.28) 169 (8.85)
0 (0.541)
August
September
651 (63.1) 3848 (70.2) 0 (19.6) 1080 (18.1) 0 (5.14) 28 (1.41) 101 (5.32)
544 (7.24)
2048 (60.7) 2151 (70.5) 37 (14.2) 133 (16.4) 0 (6.92) 0 (8.03) 72 (10.2)
Values in parenthesis represent percentages of larval nematodes. These third stage larvae were cultured and identified from faecal samples.
October 894 (69.2) 101 (21.4) 72 (0.03) 4083 (5.16)
November
28 (9.12)
2218 (66.9) 1095 (64.1) 28 (18.5) 12 (17.3) 528 (0.037) 0 (0.579)
261 (0.509) 1034 (9.75)
December
941 (67.1) 2974 (64.2) 169 (17.1) 48 (17.6) 275 (0.056) 28 (6.52)
3806 (7.38)
143 (7.58) 529 (64.0) 37 (17.4) 304 (3.66) 116 (7.91)
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
Table 2 Back-transformed mean values of gastrointestinal adult nematode counts and larval nematode percentages of dairy goats from flocks in northern and central Greece
199
200
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
percentages, therefore they were not included in the statistical analysed.
4. Discussion The comprehensive knowledge of the epizootiology of parasitism is a crucial requirement to the sustainable control of nematodes, as it interacts with the host in a specific climatic, management and production environment (Almeria and Uriarte, 1999; Waller, 1999). Anthelmintic resistance of nematode parasites of sheep and goats is present world-wide, including Greece (Papadopoulos et al., 2001), and threatens the future viability of small ruminant production in many countries (Jackson, 1993; Waller, 1999; Hoste et al., 2001). This high incidence of anthelmintic resistance is forcing people either to adopt alternative control strategies or to greatly modify the existing ones. The design of successful sustainable parasite control programmes requires knowledge of the dynamics of egg shedding from the host, seasonal larval availability together with information about climatic requirements for worm egg hatching, larval development and survival at pasture (Barger, 1999; Stromberg and Averbeck, 1999; Nginyi et al., 2001). In our study, sheep and goats from both areas were expelling nematode eggs throughout the studied period. However, this egg output was significantly different between different months of the year. Sheep from both areas of Greece had significantly higher FEC than goats. The peak of FEC of sheep was observed in April and March for northern and central Greece, respectively. This peak was noted earlier than the ones reported in other regions of northern and central Greece (Theodoropoulos et al., 1998, 2000), where FEC peaks were observed during summer. This might be due to local management differences in those areas or to different susceptibility to nematode infection of sheep used in those experiments. In our study, the intensity of infection with GI nematodes in both sheep and goats started to increase after February and the highest FEC were observed during spring. This might be associated with the post-partum or spring egg rise. However, the subsequent decrease of FEC may be affected by the development of host immunity, as a result of better nutrition during spring and the beginning of summer, or it might be related, especially to
younger animals, to the level of larval ingestion which is conditioned by the host feeding behaviour during grazing. A second but smaller peak of FEC, for both sheep and goats, was observed in October. In our view, the latter might be due to the re-infection of animals because of increased rainfall during this season that provided a more suitable environment for the survival of nematodes infective larvae, which consequently became a source of infection for the grazing animals. This higher faecal egg production during spring and autumn is well correlated with increased rainfall, particularly in central Greece, and therefore the presence of green vegetation. On the other hand, during the hot and dry summer the animals have to face the shortage of the green vegetation, which however is associated with less risk of GI nematode infection because larvae do not easily survive under such climatic conditions. Hence, it seems that rainfall is likely to be more closely correlated with the level of GI nematode parasitism than other factors, such as flock management (Cabaret et al., 1989; Niezen et al., 1996). Based on results of both the coprocultures and necropsies, we suggest that Teladorsagia is the most prevalent worm genus present throughout the year in both areas of Greece, and therefore plays an important role in the parasitic gastroenteritis together with Trichostrongylus spp., Haemonchus spp. and Chabertia spp. The less prevalent genera were Cooperia, Nematodirus and Oesophagostomum. The parasites recovered in our study have been previously reported in other surveys taken place in Greece (Theodoridis and Himonas, 1990; Papadopoulos, 1997; Theodoridis et al., 2000; Theodoropoulos et al., 2000; Papadopoulos et al., 2001). It is worth noting that in Greece, up to now, only T. circumcincta has been found to be anthelmintic resistant (Papadopoulos et al., 2001). Anthelmintic treatments of small ruminants in Greece are carried out usually once or twice per year. The present data could provide a concise epizootiological picture of gastrointestinal strongyles of small ruminants in Greece, and based on these finding we can make some recommendations regarding the anthelmintic treatment of grazing animals. The most appropriate time for treatment, according to our findings, seems to be the end of winter—beginning of spring before the peak of FEC occurs. Treatment at this time will also prevent the development of disease and any clinical symptoms in either ewes or lambs.
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
It should be noted here that under traditional small ruminant production systems in Greece, animals are not separated according to age groups but are reared together as a flock. The benefits of treating ewes at parturition, when milk is consumed by new-borns or earlier during dry period (pregnancy) are higher milk production and avoidance of withdrawal periods of milk due to drug residues period. If second treatment is needed, then treating animals during summer, when due to the drought the only surviving worms are the ones in the host, might offer a good chance to kill these worms. Furthermore, this would allow minimum contamination of the pasture and prevent the build up of worm burdens in the hosts. Nevertheless, in the latter case, it is important to note that care should be taken since the selection pressure for anthelmintic resistance is higher and any treatment should be applied with caution. According to our results, goats do not have high FEC, and therefore seem not to urgently need any anthelmintic treatment at all. We suggest that the observed differences in the FEC between sheep and goats might be due to host susceptibility and grazing behaviour of such animals (Hoste et al., 2001). Results of the current study provide a further understanding of the factors associated with parasite epizootiology and the relationship between the parasites and their host. Such information could be useful for the development of strategic treatments when sheep and goats are reared under systems similar to those described in this study.
Acknowledgements The work was supported by the European Commission (DG VI) project No. FAIR 3-CT96-1485, as part of a collaborative programme between the UK, France, Greece and Spain. We would like to thank Dr. D. Allcroft of SAC, Edinburgh, for his helpful comments on how to improve the manuscript. References Almeria, S., Uriarte, J., 1999. Dynamics of pasture contamination by gastrointestinal nematodes of cattle under extensive management systems: proposal for strategic control. Vet. Parasitol. 83, 37–47.
201
Barger, I., 1999. The role of epidemiological knowledge and grazing management for helminth control in small ruminants. Int. J. Parasitol. 29, 41–47. Cabaret, J., Anjorand, N., Leclerc, C., 1989. Parasitic risk factors on pastures of French dairy goat farms. Small Rumin. Res. 2, 69–78. FAOSTAT, 2001. FAO Agriculture Statistical Database. Hoste, H., Leveque, H., Dorchies, Ph., 2001. Comparison of nematode infections of the gastrointestinal tract in Angora and dairy goats in a rangeland environment: relations with the feeding behaviour. Vet. Parasitol. 101, 127–135. Jackson, F., 1993. Anthelmintic resistance—the state of play. Brit. Vet. J. 149, 123–138. Jackson, F., Coop, R.L., 2000. The development of anthelmintic resistance in sheep nematodes. Parasitology 120, S95–S107. Lawes Agricultural Trust, 1993. Genstat 5 Release 3.2 Reference Manual, 2nd ed. Clarendon Press, Oxford. Ministry of Agriculture Fisheries and Food (MAFF), 1986. Manual of Veterinary Parasitological Laboratory Techniques. Reference Book 418. HMSO, London. Nginyi, J.M., Duncan, J.L., Mellor, D.J., Stear, M.J., Wanyangu, S.W., Bain, R.K., Gatongi, P.M., 2001. Epidemiology of parasitic gastrointestinal nematode infections of ruminants on smallholder farms in central Kenya. Res. Vet. Sci. 70, 33– 39. Niezen, J.H., Charleston, W.A.G., Hodgson, J., McKay, A.D., Leathwick, D.M., 1996. Controlling internal parasites in grazing ruminants without recourse to anthelmintics: approaches, experiences, prospects. Int. J. Parasitol. 26, 983–992. Papadopoulos, E., 1997. Anthelmintic resistance of sheep and goat gastrointestinal nematode parasites in Greece. Doctoral thesis, Aristotle University of Thessaloniki, Greece. Papadopoulos, E., Himonas, C., Coles, G.C., 2001. Drought and flock isolation may enhance the development of anthelmintic resistance in nematodes. Vet. Parasitol. 97, 89–93. Stromberg, B., Averbeck, G., 1999. The role of parasite epidemiology in the management of grazing cattle. Int. J. Parasitol. 29, 33–39. Sykes, A.R., 1994. Parasitism and production in farm animals. Anim. Prod. 59, 155–172. Thamsborgh, M.S., Roepstorff, A., Larsen, M., 1999. Integrated and biological control of parasites in organic and conventional production systems. Vet. Parasitol. 84, 169–186. Theodoridis, Y., Himonas, C., 1990. A survey on the specific aetiology of sheep and goats gastrointestinal nematodosis. In: Proceedings of the Fifth Hellenic Veterinary Congress, Thessaloniki, Greece, 22–25 November 1990, pp. 96–98 (Abstract No. E-6). Theodoridis, Y., Himonas, C., Papazahariadou, M., 2000. Helminths parasites of digestive tract of sheep and goats in Macedonian region. Bull. Hellenic Vet. Med. Soc. 51, 195–199. Theodoropoulos, G., Koutsotolis, K., Nikolaou, E., Kalogiannis, D., Petrakos, G., 1998. Seasonal variation of gastrointestinal nematodes of sheep in the region of Joannina, Greece. Int. J. Parasitol. 28, 1287–1292. Theodoropoulos, G., Zervas, G., Kouneli, A., Martinez-Gonzales, B., Petrakos, G., Kostopoulos, J., 2000. Seasonal patterns of
202
E. Papadopoulos et al. / Small Ruminant Research 47 (2003) 193–202
strongyle infections in grazing sheep under the traditional production system in the region of Trikala, Greece. Vet. Parasitol. 89, 327–335. Waller, P.J., 1997. Anthelmintic resistance. Vet. Parasitol. 72, 391– 412. Waller, P.J., 1999. International approaches to the concept of integrated control of nematode parasites of livestock. Int. J. Parasitol. 29, 155–164.
Zygoyiannis, D., 1999. Sheep Production. Modern Education, Thessaloniki. Zygoyiannis, D., Katsaounis, N., 1994. Goat Production. Modern Education, Thessaloniki. Zygoyiannis, D., Katsaounis, N., Stamataris, C., Arsenos, G., Tsaras, L., Doney, J., 1999. The use of nutritional management after weaning for the production of heavier lamb carcasses from Greek dairy breeds. Livest. Prod. Sci. 57, 279–289.